Open Access
17 May 2016 Short-term pulse rate variability is better characterized by functional near-infrared spectroscopy than by photoplethysmography
Lisa Holper M.D., Erich Seifritz M.D., Felix Scholkmann
Author Affiliations +
Abstract
Pulse rate variability (PRV) can be extracted from functional near-infrared spectroscopy (fNIRS) (PRVNIRS) and photoplethysmography (PPG) (PRVPPG) signals. The present study compared the accuracy of simultaneously acquired PRVNIRS and PRVPPG, and evaluated their different characterizations of the sympathetic (SNS) and parasympathetic (PSNS) autonomous nervous system activity. Ten healthy subjects were recorded during resting-state (RS) and respiratory challenges in two temperature conditions, i.e., room temperature (23°C) and cold temperature (4°C). PRVNIRS was recorded based on fNIRS measurement on the head, whereas PRVPPG was determined based on PPG measured at the finger. Accuracy between PRVNIRS and PRVPPG, as assessed by cross-covariance and cross-sample entropy, demonstrated a high degree of correlation (r<0.9), which was significantly reduced by respiration and cold temperature. Characterization of SNS and PSNS using frequency-domain, time-domain, and nonlinear methods showed that PRVNIRS provided significantly better information on increasing PSNS activity in response to respiration and cold temperature than PRVPPG. The findings show that PRVNIRS may outperform PRVPPG under conditions in which respiration and temperature changes are present, and may, therefore, be advantageous in research and clinical settings, especially if characterization of the autonomous nervous system is desired.

1.

Introduction

Heart rate variability (HRV), i.e., the variations in the inter-beat-interval of the heart rate (HR), is a physiological phenomenon. The usefulness of HRV as a tool for basic research as well as for medical diagnostic purposes to assess the function of the autonomic nervous system has been verified in numerous studies.14 The gold standard is the analysis of interbeat (RR) intervals derived from electrocardiography (ECG). Alternatively, pulse cycle intervals variability based on blood flow pulsations (i.e., PRV) can be derived from pulse oximetry, i.e., photoplethysmography (PPG) (PRVPPG). PRVPPG is convenient, noninvasive, and widely available and has, therefore, been suggested for simplifying ambulatory HRV monitoring.57 Under resting conditions, recordings derived from PPG and ECG demonstrate a high degree of correlation (r>0.93).7,8 However, PRVPPG also has disadvantages. While sufficient accuracy can be obtained when subjects are under optimal resting conditions, PRVPPG has been reported to be vulnerable to motion artifacts,6 physical exercise,5 or mental stressors,7 making it considerably less accurate compared to ECG. The smaller accuracy may arise due to probe instability, sweating, artifacts during exercise, and the influence of different cardiovascular components. Furthermore, the accuracy has been reported to particularly decrease for high frequency (HF) or short-term variability; in other words, PRVPPG has been shown to have a smaller accuracy in particular for the contributions of the parasympathetic nervous system (PSNS)7,9 compared to the HRV derived from ECG.

The sympathetic nervous system (SNS) and PSNS have profound impacts on HRV and thus PRV. For example, decreased SNS activity or increased PSNS activity typically results in a reduction versus an increase of HRV. To characterize the contributions of the SNS and PSNS on HRV and PRV, frequency-domain methods have been typically applied. Activity in the HF band (0.15 to 0.40 Hz) can be associated with increased PSNS activation. For example, variation of HF can be driven by respiratory changes that modulate HRV and PRV via increases or decreases in PSNS activity.1012 Similarly, exposure to cold temperature leads to a reduction in HRV and PRV via increased PSNS activity in order to save and restore body energy. The relationship between the HF component and the PSNS state is thereby mainly caused by the cardiac PSNS’s input and thus not directly reflects the parasympathetic “tone” per se.13 Activity in the low frequency (LF) band (0.04 to 0.15 Hz), in contrast, in thought to represent a mixture of the modulation of both SNS and PSNS.14 Therefore, the ratio between LF and HF (LF/HF ratio) has been suggested to reflect an approximation of the association between SNS and PSNS.1517 However, recent studies reported that the LF/HF ratio does not accurately measure cardiac SNS-PSNS balance.14,18,19 Based on this, the SDNN/RMSSD has been proposed as another surrogate measure for the LF/HF ratio in the time-domain.20 Whereas SDNN (i.e., the standard deviation of normal to normal RR intervals) is thought to represent characteristics of long-term HRV and PRV changes, RMSSD (i.e., the root mean square of successive heartbeat interval differences) is associated with short-term HRV and PRV changes. The SDNN/RMSSD ratio is, therefore, thought to represent the balance between long-term and short-term variabilities and thus represents the SNS-PSNS balance.21

The two described measures can be related to one of the most commonly used method for analyzing HRV and PRV, i.e., Poincaré plots. Poincaré plots are graphical illustrations of two consecutive RR intervals and are valuable due to their ability of displaying the nonlinear aspects of HRV and PRV sequences.22 The typical elongated shape of a Poincaré plot can be evaluated numerically using an ellipse fitting technique that provides a ratio of two standard deviations, i.e., the ratio between the dispersion (standard deviation) on the minor axis (SD1) and on the major axis (SD2), called the SD1/SD2 ratio. Whereas SD1 represents the short-term HRV and PRV thought to reflect PSNS activity, SD2 represents the long-term HRV and PRV thought to reflect SNS activity, with the SD1/SD2 ratio denoting the SNS-PSNS balance.

Finally, based on the SD1 and SD2 parameters, yet another measure has been recently proposed, the complex correlation measure (CCM).23,24 CCM is a nonlinear HRV and PRV measure that quantifies the temporal aspects of Poincaré plots. In contrast to SD1 and SD2, CCM measures the beat-to-beat dynamics and is particularly thought to have a greater sensitivity to changes in PSNS activity.

In the present analysis, we aimed to apply the described linear and nonlinear measures to examine the accuracy and characterize the contributions of the SNS and PSNS of PRVPPG in comparison to PRV derived from functional near-infrared spectroscopy (fNIRS) (PRVNIRS).

So far, PRV quantitation using fNIRS has been investigated in two studies. Trajkovic et al.25 quantified the correlation between PPG (and HRV, respectively) signals derived from simultaneously acquired fNIRS and ECG in 11 healthy adults and reported a high correlation (r>0.98). Perdue et al.26 investigated simultaneously acquired fNIRS-based pulse activity and ECG-based heart activity in 10 healthy infants and reported not only a high correlation during the RS (median  r=0.90), but also during visual stimulation (median  r=0.981), despite high levels of movements typically occurring in infants.

To characterize the contributions of the SNS and PSNS on the PRV, the present study assessed the impact of changes in respiration and temperature on the PRV, which are both important variables affecting PRV via the SNS and PSNS.27 Changes in respiration were induced by respiratory challenges, i.e., hyperventilation (HV), breath-holding (BH), and rebreathing (RB) compared to RS. Changes in temperature were induced by changing the environmental (i.e., room) temperature (23°C versus 4°C). PRVNIRS was measured on the head and PRVPPG was measured on the finger.

By addressing both the accuracy and contributions of the autonomic nervous system, we hypothesized to provide meaningful information on the performance of PRVNIRS and PRVPPG. In particular, we hypothesized that both changes in respiration and temperature would elicit larger short-term variability (HF, RMSSD, and SD1) reflecting increased PSNS activity, and that PRVNIRS may characterize these changes better compared to PRVPPG, due to the known drawbacks of motion artifacts in PRVPPG. Extracting PRVNIRS may further be advantageous for both research and clinical settings, as fNIRS is a brain imaging method at the same time, which would enable to measure both brain activity and PRV simultaneously.

2.

Materials and Methods

2.1.

Subjects

Ten healthy subjects (age 32±2.3 years, five females) were recruited at the University of Zurich. Exclusion criteria were any psychiatric or neurological disorder or current medication. All subjects gave written informed consent. The study was approved by the ethics committee of the Canton Zurich (KEK-ZH-Nr: 2014-0056) and conducted in accordance with the Declaration of Helsinki.

2.2.

Experimental Protocol

Each subject underwent two experimental series separated by 1 week. Both experimental conditions were conducted at the same day and time between 9:00 and 12:00 am with a total duration of 10 min. Subjects were seated in a comfortable chair with the head positioned in a head rest in order to minimize head motion; this postural position was maintained during the whole experiment.

  • CONTROL temperature: The first experimental series was conducted at a room temperature of 23°C.

  • COLD temperature: The second experimental series was conducted at a cold temperature of 4°C within a cold storage room.

In both temperature conditions, subjects wore regular street wear and there was no other difference in the setup between the conditions. The following four respiratory challenges were assessed in each condition:

  • RS (5 min) consisted of subjects sitting still with eyes open with normal breathing (60 s break interval, 15  cycles/min).

  • HV consisted of one period of rapidly breathing in and out with constant respiratory volume (30 s, 60  cycles/min) followed by normal breathing (60 s break interval).

  • BH consisted of one period of breath hold (30 s, no breathing) followed by normal breathing (60 s break interval).

  • RB consisted of one period of breathing in an RB bag (3 L) (30 s, respiration rate did not differ from normal breathing, i.e., 15  cycles/min) followed by normal breathing (60 s break interval).

For BH and RB, subjects were trained prior to recording to perform the inspirational volume of air before the challenge similar to a normal breath cycle, in order to avoid inhaling a larger volume of air than the volume of a normal breath cycle.

2.3.

Functional Near-Infrared Spectroscopy Instrumentation

An NIRSport instrument (LLC NIRx Medical Technologies) was used for the fNIRS recordings. The system utilized time-multiplexed dual-wavelength light-emitting diodes. Each diode contained two light sources with wavelengths of 760 and 850 nm. Optical detection was performed with photoelectrical detectors containing silicon photodiodes (Siemens, Germany). Sources and detectors were placed in a head cap to allow for direct skin contact (Epitex Inc., Japan). The data acquisition board was connected to a notebook computer running LabVIEW 2011 (National Instruments, Austin, Texas). The fNIRS data were recorded with a sampling frequency of 7.81 Hz. The probe setup covered parts of the prefrontal cortex (Fig. 1). Functional recordings were visually inspected for motion artifacts (in particular, “steps” and “spikes”) without the need for removal of artifacts. The time series of oxyhemoglobin (O2Hb) were then used to extract HRV (Sec. 2.4).

Fig. 1

fNIRS channel positions. Channel setup covering the prefrontal cortex (channels indicate the middle between source and detector). The MATLAB® toolbox NFRI28 was used to estimate the MNI coordinates of the used EEG 10 to 20 position. Channel positions were visualized using BrainNet Viewer.29

JBO_21_9_091308_f001.png

2.4.

Pulse Rate Variability Extraction from Functional Near-Infrared Spectroscopy

PRVNIRS was extracted using the automatic multiscale-based peak detection (AMPD) algorithm developed by Scholkmann et al.30 AMPD is based on the calculation and analysis of the local HR maxima in the raw fNIRS time series. AMPD detects the HR peaks, which are then used to calculate the interpeak intervals frequency via interpolating the time difference signal. The first step of the AMPD algorithm consists of calculating the local maxima scalogram (LMS). To this end, the signal is first linearly detrended in that the least-squares fit of a straight line to a given raw O2Hb signal is calculated and subtracted from the signal. The local maxima of the signal are then determined using a moving window approach. The second step of the algorithm comprises a row-wise summation of the LMS matrix resulting in a vector v. The global minimum λ of the vector v represents the scale with the most local maxima, which is then used in the third step to reshape the LMS matrix by removing all elements larger than λ. In the last step of the algorithm, the HR peaks are detected by calculating the columnwise standard deviation of the LMS matrix. Each point of the total number of detected peaks of a given signal indicated the values of the detected peaks (Fig. 2). The AMPD calculation was done for each of the channels (i.e., 1 to 16) and for each subject. Channels without cardiac components due to noise were identified and excluded from analysis. A final PRVNIRS estimate was obtained for each single subject by computing the median PRV over all channels at each time point.

Fig. 2

PRV-extraction from fNIRS. Illustration of the results of applying the AMPD algorithm30 to raw fNIRS time series to calculate PRVNIRS. Red dots represent the detected HR peaks in a given signal with the peaks indicating the values of PRV at each point.

JBO_21_9_091308_f002.png

2.5.

Photoplethysmography-Derived Pulse Rate Variability

A LifeSense LS1-9R multiparameter instrument (Nonin Medical, Sweden) was used to derive HR from finger PPG. Subjects wore a finger pulse oximeter through which HR were sampled at 10 Hz. Triggers were logged to allow for temporal synchronization with the fNIRS data. For statistical analysis, HR values were automatically computed by the LifeSense instrument from the raw data.

3.

Data Analysis

Data collection and statistical analysis were performed in accordance with the Task Force Guidelines of The European Society of Cardiology and the North American Society of Pacing and Electrophysiology31 and the related literature.32,33

Statistical analysis was performed using MATLAB® (Version 2015b, MathWorks). All methods were applied on the single-subject level, and presented on the group-level. The analysis included the RS series (5 min), HV, BH, and RB (each 30 s). The break intervals between the respiratory challenges were not included in the analysis. Statistical significance was assessed using repeated measures ANOVA with the between-subject factor “temperature” (CONTROL versus COLD) and the within-subject factor “respiration” (RS, HV, BH, and RB). In the case of significance, a paired t-test was used as post hoc comparison. To illustrate the performance of PRVNIRS and PRVPPG, receiver operating characteristic (ROC) curves were generated based on logistic regression using the binary classifier “temperature” (CONTROL versus COLD). The significance level was considered to be p<0.05.

3.1.

Accuracy Between Pulse Rate Variability Measures

3.1.1.

Cross-covariance

Normalized cross-covariance (C-COV) was quantified to assess the accuracy between PRVNIRS and PRVPPG as suggested by Perdue et al.26 The covariance was scaled; hence, the auto-covariance was 1 for each signal at time lag 0. The time lag between the two traces was allowed to vary, and the highest correlation coefficient (r) was reported. Coefficients higher than r>0.3 were considered moderate, coefficients higher than r>0.7 were considered large. A mean time lag of 0.4±4.6  s was found between PRVNIRS and PRVPPG. The smallest time lags were observed in the RS, but there were overall no significant lag-differences between the RS, the respiratory challenges, or the temperature change. Perdue et al.26 suggested that this delay is due to the slow hemodynamic response time that may vary between subjects and may be dependent upon variations in subject blood vessels.

3.1.2.

Cross-sample entropy

Cross-sample entropy (C-SampEn) was applied as a nonlinear measure to quantify the regularity or synchronicity in the potentially nonstationary PRV signals.34 Entropy-based measures have been widely used for the analysis of physiological time series to explore the complexity between two time-series.35,36 C-SampEn measures the relative regularity of two signals, with lower C-SampEn values denoting greater conditional regularity or synchronicity, whereas higher values implicate that the given signals are less predictable (or more complex). While C-SampEn may be intuitively understood as the opposite of temporal correlation, it does not assume that signals are temporally stationary processes, but provides an alternative and complementary measure to assess the nonlinear statistics of PRV.3739

3.2.

Sympathetic and Parasympathetic Autonomous Nervous System Contributions on Pulse Rate Variability

The following measures of short-term and long-term variabilities were assessed only in the RS series. The respiratory challenges were analyzed only with respect to the short-term variability (see rationale in Secs. 3.2.1 and 3.2.2).

3.2.1.

Frequency-domain (low frequency/high frequency ratio)

Power spectral density (PSD) in the frequency-domain was applied to calculate the averaged power in the HF band (0.15 to 0.4 Hz) and the LF band (0.04 to 0.15 Hz). We applied the Lomb-Scargle power spectral density (LS-PSD) estimate that has been proposed as a more appropriate method for HRV compared to classical fast Fourier transform-based methods,40 since it can be used without the need to resample and to detrend the typically unevenly sampled HRV time series.

PSD only provides an accurate estimation when the signal is supposed to maintain stationarity, which typically requires long-term recordings. Recordings should be at least 10 times the wavelength of the lowest frequency bound of interest. Thus, recordings of 1  min are needed to assess the HF components (i.e., a lowest bound of 0.15 Hz is a cycle of 6.6 s, therefore 10 cycles require 60  s), while more than 4 min are needed to address the LF component (with a lower bound of 0.04 Hz). In the present analysis, we, therefore, only analyzed the RS series (5 min, consisting of at least 256 samples32).

3.2.2.

Time-domain (SDNN/RMSSD ratio)

As suggested by Wang and Huang,20 the two surrogate indices, SDNN and RMSSD, in the time-domain were computed. Analysis was performed using the HRVAS toolbox.41 Analog to the frequency-domain, very short time series may not provide an accurate estimate of SDNN,42,43 therefore, the present analysis focused only on the RS series (5 min).

3.2.3.

Poincaré plot (SD1/SD2 ratio)

Poincaré plots were constructed as a delay scatter plot between the intervals RRi (x-axis) and RRi+1 (y-axis), with each point in the plot corresponding to two consecutive RR intervals.22,44 The Poincaré shapes representing an elongated cloud of points (Fig. 5) around the line-of-identity were evaluated numerically using the ellipse fitting technique. The minor axis of the ellipse perpendicular to line-of-identity is the standard deviation SD1, whereas the major axis is represented by the standard deviation SD2. Analysis was performed using the HRVAS toolbox41 based on only the RS series (5 min).

3.2.4.

Complex correlation measure

The complex correlation method (CCM) was applied to quantify the nonlinear temporal aspects of the Poincaré plot.23,24 CCM was computed in a windowed manner, which embeds the temporal information of the signal. A moving window of three consecutive points obtained from the Poincaré plot was considered to measure the temporal variation of the points. The detailed mathematical formulation has been previously reported.23

4.

Results

4.1.

Pulse Rate Variability Near-Infrared Spectroscopy and Photoplethysmography

Extraction of PRVNIRS was performed for each of the fNIRS channels 1 to 16 per subject. 13% of the channels over all subjects did not contain cardiac components due to a low signal-to-noise ratio and were excluded from analysis. A single-subject example of the final PRVNIRS estimate obtained by computing the median PRV over all channels at each time point is shown in Fig. 3(a) in comparison to PRVPPG.

Fig. 3

PRNIRS and PRPEG. (a) Single-subject examples illustrating raw time courses of HRNIRS and HRPPG. (b) Group-level beta estimates of HR responses to respiratory challenges, HV, BH, and RB. Error bars indicate standard error of the mean (SEM). Significance between temperature conditions was highlighted (*).

JBO_21_9_091308_f003.png

Using a general linear model, the beta estimates of the HR in response to the respiratory challenges were calculated per subject and shown on the group-level [Fig. 3(b)]. Results showed that compared to RS, HV (PRVNIRS: p<0.001, PRVPPG: p<0.046) and RB (PRVNIRS: p<0.009, PRVPPG: p<0.0001) induced a larger increase in HR in the CONTROL condition compared to the COLD condition, whereas BH (PRVNIRS: p=0.044, PRVPPG: p<0.0001) induced a smaller HR decrease in condition CONTROL compared to condition COLD. These results indicated that the HR response was overall diminished in the COLD compared to the CONTROL condition.

4.2.

Accuracy Between Pulse Rate Variability Measures

The overall correlation between PRVNIRS and PRVPPG was r>0.9. The accuracy between PRVNIRS and PRVPPG was assessed using C-COV and C-SampEn (Fig. 4). Repeated measures ANOVA showed a consistent pattern with significant main effects for both factors “temperature” and “respiration” (Table 1). The between-subject factor “temperature” (CONTROL versus COLD) revealed a smaller main effect for C-COV (F=10.026, p=0.005) compared to C-SampEn (F=52.134, p<0.0001). The within-subject factor “respiration” (RS, HV, BH, and RB) revealed larger C-COV correlation coefficients between PRVNIRS and PRVPPG in the RS in the CONTROL (r=0.903) compared to the COLD (r=0.803) condition. During the respiratory challenges, correlation coefficients decreased with the smallest values in response to BH under both the CONTROL and the COLD condition. Sample entropy represented a mirrored pattern of the correlation analysis, but with an overall larger “temperature” effect, but smaller effects of “respiration” indicating less variance between the respiratory challenges.

Fig. 4

C-COV and C-SampEn. Group-level results of the accuracy between PRVNIRS and PRVPPG assessed using C-COV and C-SampEn. Error bars indicate SEM. Significant differences between temperature conditions were highlighted (*). See Table 1 for ANOVA.

JBO_21_9_091308_f004.png

Table 1

ANOVA C-COV and C-SampEn. Repeated measures ANOVA assessing the accuracy between PRVNIRS and PRVPPG using C-COV and C-SampEn, with the between-subject factor “temperature” (CONTROL versus COLD) and the within-subject factor “respiration” (RS, HV, BH, and RB), followed by post-hoc comparisons using paired-test. See Fig. 4 for illustration.

CONTROLCOLDCONTROL versus COLD
Main effect “respiration”F=0.025F=8.285Main effect “temperature”F=10.026
p=0.877p=0.018p=0.005
ηp2=0.003ηp2=0.479ηp2=0.358
C-COVRS versus HV0.6740.579RS0.039
RS versus BH0.8720.024HV0.154
RS versus RB0.8660.209BH0.005
HV versus BH0.9310.013RB0.033
HV versus RB0.7210.116
BH versus RB0.6370.327
Main effect “respiration”F=28.698F=8.029Main effect “temperature”F=52.134
p<0.001p=0.020p<0.0001
ηp2=0.761ηp2=0.471ηp2=0.743
C-SampEnRS versus HV0.0010.308RS0.000
RS versus BH0.0250.190HV0.094
RS versus RB0.0000.030BH0.005
HV versus BH0.3830.790RB0.004
HV versus RB0.9270.126
BH versus RB0.3230.511

4.3.

Sympathetic and Parasympathetic Autonomous Nervous System Contributions on Pulse Rate Variability

4.3.1.

Frequency-domain (low frequency/high frequency ratio)

To investigate the frequency aspects that may characterize the contributions of the SNS and PSNS, the HF (0.15 to 0.4 Hz) and LF (0.04 to 0.15 Hz) activities were assessed. Results from the RS indicated that the COLD condition elicited an overall smaller LF/HF ratio compared to the CONTROL condition (Fig. 5). The difference was significant only for PRVNIRS (p<0.018), but not for PRVPPG (p=0.829). The proportional change from the CONTROL to COLD condition was larger in HF activity (76.48%) compared to LF activity (25.48%) (Table 2), indicating that higher HF activity under the COLD condition was the main proportional contributor to the statistical difference. Results obtained from the respiratory challenges showed that the difference in HF activity reached statistical significance only for PRVNIRS for all challenges, but not for PRVPPG (Fig. 6).

Fig. 5

PRVNIRS and PRVPPG measures (RS). (a) Single-subject level. Examples of the PRV measures assessed in the frequency-domain, the time-domain, the Poincaré plot, and the CCM. (b) Group-level. Bar graphs illustrating the mean±SEM of the LF/HF ratio, the SDNN/RMSSD ratio, the SD1/SD2 ratio, and the CCM. Significant differences between temperature conditions were highlighted (*). See Table 2 for statistics.

JBO_21_9_091308_f005.png

Table 2

PRVNIRS and PRVPPG measures (RS). Mean/median±SEM of LF, HF, SDNN, RMSSD, SD1, SD2, and CCM. Differences between the CONTROL and the COLD condition were assessed using paired t-test. Units are given in milliseconds.

CONTROLCOLDT-testProportional change (mean)
MeanSEMMedianMeanSEMMedianFp-value
Frequency-domainPRVNIRSLF2852.753588.5692514.7003579.560640.6513093.0000.6980.41425.48%
HF156.34334.445130.115275.92158.104217.9253.1340.09476.48%
PRVPPGLF484.16480.638390.130477.207137.414328.0950.0020.9661.44%
HF21.3441.53121.42222.7386.74712.3800.0410.8436.53%
PRVNIRSLF/HF ratio18.3991.0901869.18114.0161.2751348.5466.8260.018
PRVPPGLF/HF ratio22.0852.9031851.05021.2542.4262331.7230.0480.829
Time-domainPRVNIRSSDNN102.09013.57982.350106.42016.210106.2500.0420.8404.24%
RMSSD3.3300.3393.3004.2500.5083.6502.2710.14927.63%
PRVPPGSDNN40.0805.71437.15040.5403.55637.9500.0050.9461.15%
RMSSD1.1800.1061.1331.2600.1381.1500.2120.6516.78%
PRVNIRSSDNN/RMSSD ratio30.2181.77228.84324.5331.88422.7554.8340.041
PRVPPGSDNN/RMSSD ratio33.1171.88631.21734.1063.38632.0250.0650.801
Poincaré plotPRVNIRSSD10.0030.0000.0030.0040.0010.0030.5710.46018.22%
SD20.1330.0110.1190.1140.0200.0790.7050.41214.31%
PRVPPGSD10.0010.0000.0010.0010.0000.0010.0070.9321.52%
SD20.0520.0060.0480.0550.0040.0540.1790.6785.87%
PRVNIRSSD1/SD2 ratio0.0220.0020.0230.0320.0030.03111.2040.004
PRVPPGSD1/SD2 ratio0.0180.0010.0170.0170.0020.0150.1640.690
CCMPRVNIRSCCM0.0030.0000.0030.0050.0010.0054.4920.047
PRVPPGCCM0.0040.0000.0040.0040.0000.0040.0620.806

Fig. 6

PRVNIRS and PRVPPG measures (respiratory challenges). Bar graphs illustrating the mean±SEM of the short-term variability measures, HF, RMSSD, and SD1, during HV, BH, and RB, for PRVNIRS and PRVPPG. Significant differences between temperature conditions were highlighted (*).

JBO_21_9_091308_f006.png

4.3.2.

Time-domain (SDNN/RMSSD ratio)

Results from the RS in the time-domain indicated that the COLD condition elicited an overall smaller SDNN/RMSSD ratio compared to the CONTROL condition (Fig. 5). The difference was significant only for PRVNIRS (p=0.041), but not for PRVPPG (p=0.801). The proportional change from the CONTROL to COLD condition was larger in RMSSD (27.63%) compared to SDNN (4.24%) (Table 2), indicating that a higher RMSSD index in the COLD condition was the main proportional contributor to the statistical difference. Results obtained from the respiratory challenges showed that the difference in the RMSSD index reached statistical significance only for PRVNIRS for all challenges, but not for PRVPPG (Fig. 6).

4.3.3.

Poincaré plot (SD1/SD2 ratio)

Results from the RS of the Poincaré plot revealed that the COLD condition elicited a larger SD1/SD2 ratio compared to the CONTROL condition (Fig. 5). Again, the difference was significant only for PRVNIRS (p=0.004), but not for PRVPPG (p=0.690). The proportional change from the CONTROL to COLD condition was larger in SD1 (18.22%) compared to SD2 (14.31%) (Table 2), indicating that a higher SD1 index in the COLD condition was the main proportional contributor to the statistical difference. Results obtained from the respiratory challenges showed that the difference in the SD1 index reached statistical significance only for PRVNIRS for all challenges, but not for PRVPPG (Fig. 6).

4.3.4.

Complex correlation measure

The CCM was calculated based on the SD1 and SD2 derived from the Poincaré plot.23 Results from the RS revealed that the COLD condition elicited a larger CCM value compared to the CONTROL condition (Fig. 5). Again, this difference was significant only for PRVNIRS (p=0.047), but not for PRVPPG (p=0.806).

4.3.5.

Receiver operating characteristic for pulse rate variability measures

To illustrate the performance of PRVNIRS and PRVPPG in predicting the temperature change, ROC curves were generated based on logistic regression with the binary classifier “temperature” (CONTROL versus COLD) and the PRV measures as response variables. The AUC values obtained from the RS showed that PRVNIRS predicted the temperature change better than PRVPPG for all measures, i.e., the LF/HF ratio, the SDNN/RMSSD ratio, the SD1/SD2 ratio, and the CCM (Fig. 7). The differences between AUC reached significance level only for the SD1/SD2 ratio p<0.0001 (LF/HF ratio p=0.054, SDNN/RMSSD ratio p=0.069, and CCM p=0.224). Results obtained from the respiratory challenges confirmed these findings, showing that the AUC values for HF activity, RMSSD, and SD1 were larger for PRVNIRS for most of the challenges compared to PRVPPG (exceptions see Fig. 8).

Fig. 7

ROC for PRVNIRS and PRVPPG (RS). Group-level ROC curves and AUC values based on logistic regression with the binary classifier “temperature” (CONTROL versus COLD) for each of the PRV measures, the LF/HF ratio, the SDNN/RMSSD ratio, the SD1/SD2 ratio, and the CCM. Statistical significance of AUC-differences: LF/HF-ratio p=0.054, SDNN/RMSSD ratio p=0.069, SD1/SD2 ratio p<0.0001, CCM p=0.224.

JBO_21_9_091308_f007.png

Fig. 8

ROC for PRVNIRS and PRVPPG (respiratory challenges). Group-level ROC curves and AUC values based on logistic regression with the binary classifier “temperature” (CONTROL versus COLD) for each of the short-term variability measures, HF, RMSSD, SD1, during HV, BH, and RB, for PRVNIRS and PRVPPG. Statistical significance of AUC-differences in HV: HF p=0.009, RMSSD p=0.015, SD1 p=0.011; statistical significance of AUC-differences in BH: HF p<0.0001, RMSSD p<0.0001, SD1 p<0.0001; statistical significance of AUC-differences in RB: HF p=0.285, RMSSD p=0.091, SD1 p<0.0001.

JBO_21_9_091308_f008.png

4.3.6.

Correlation between pulse rate variability measures

Pearson correlation coefficients were computed between LF, HF, SDNN, RMSSD, SD1, SD2, and CCM values, for the COLD and CONTROL condition (Fig. 9). Results confirmed that the indices of short-term variability (HF, RMSSD, and SD1) and long-term variability (LF, SDNN, and SD2) exhibited a strong positive correlation each other, and a negative correlation with CCM. The correlations were less stable for PRVPPG under the COLD condition. Results obtained from the respiratory challenges are shown in the Fig. 10.

Fig. 9

Correlation between PRV measures (RS). Pearson correlation coefficients for PRVNIRS and PRVPPG between LF, HF, SDNN, RMSSD, SD1, SD2, and CCM values, for the CONTROL and the COLD conditions.

JBO_21_9_091308_f009.png

Fig. 10

Correlation between PRV measures (respiratory challenges). Pearson correlation coefficients for PRVNIRS and PRVPPG between the short-term variability measures, HF, RMSSD, and SD1, for the CONTROL and the COLD conditions.

JBO_21_9_091308_f010.png

5.

Discussion

Previous studies showed that information on the temporal inter-beat-intervals of the heart can be extracted from fNIRS data.25,26 By comparing simultaneously acquired PRV from NIRS (PRVNIRS) and PRVPPG, the present study showed that PRVNIRS may outperform PRVPPG under conditions involving respiratory and temperature changes. In particular, we show that PRVNIRS may provide a better characterization of the contributions of the SNS and parasympathetic autonomous nervous system compared to PRVPPG, especially regarding the short-term variability. Extracting PRVNIRS may, therefore, be advantageous for both research and clinical settings as an alternative to PRVPPG.

A main methodological limitation of the present study was that we did not assess simultaneous ECG, the gold standard for investigating PRV. This limitation should be considered when interpreting our results. In 1996, a task force31 specified standards for calculating PRV measures and reporting results, which have been considered in the present study. Accuracy of the ECG has since then been investigated in numerous studies in health and disease,14 and the correlation with both PRVPPG7 and PRVNIRS25 under resting conditions has been reported to be high.

5.1.

Accuracy Between Pulse Rate Variability Measures

To compare the accuracy between PRVNIRS and PRVPPG, the present analysis assessed C-COV and C-SampEn. C-COV showed the relative correlations between the PRVNIRS and PRVPPG, whereas C-SampEn reflected the regularity between the two PRV measures. Overall, we found good agreement between the two methods with the largest coefficients under RS (r=0.903). However, both changes in respiration and temperature resulted in reduced correlation (C-COV) and stronger irregularity (C-SampEn) between PRVNIRS and PRVPPG (Fig. 4 and Table 1). The lower correlation in response to respiratory and temperature changes may reflect the previously reported inaccuracy of PRVPPG under nonoptimal conditions, such as including motion artifacts,6 physical strenuous exercise,5 or mental stressors.7 Although our subjects were instructed to keep the body as still as possible during the respiratory challenges, the breathing and temperature changes certainly induced minor body motions and mental stress, respectively, that may have contributed to the inaccuracy of PRVPPG. The PRVNIRS signal shows more high-frequency variability compared to PRVPPG. That this high-frequency variability contains some physiological relevant information (i.e., diminished in the PRVPPG data) is a shown by the present results.

It should further be mentioned that the correlations between PRVNIRS and PRVPPG were slightly lower than that has been reported previously in adult25 and infant data.26 These differences may arise due the difference between PPG (applied in our study) versus EEG (applied in the two other studies).

5.2.

Sympathetic and Parasympathetic Autonomous Nervous System Contributions on Pulse Rate Variability

To characterize the contributions of the SNS or PSNS on PRVNIRS and PRVPPG in response to the temperature change, we applied frequency- and time-domain measures based on linear and nonlinear methods.

In general, exposure to cold temperature changes the relationship between the SNS or PSNS. Whereas the PSNS (the “rest and digest” system) restores the body’s energy primarily associated with decreases in PRV, the SNS (the “fight and flight” system) is primarily associated with increases in PRV. Furthermore, although the effect on PRV of cooling varies with the duration of the temperature change, it is thought that cold exposure modulates short-term variability (i.e., HF, RMSSD, and SD1) more than long-term variability (LF, SDNN, and SD2).8 This indicates that cold exposure modulates SNS-PSNS balance by causing a shift toward increased PSNS activity. Previous studies comparing PRV derived from PPG and ECG under optimal rest conditions did not report significant differences in PRV assessment.6,45,46 However, studies that compared PPG and ECG under less optimal conditions have shown that PRVPPG assessed the parameters of short-term variability (HF, RMSSD, and SD1) considerable less reliable compared to ECG.7,9

In line with these findings, our results showed that the cold temperature change (COLD) exhibited significant increases of the parameters reflecting short-term variability (i.e., HF activity, RMSSD, and SD1), whereas the parameters reflecting long-term variability did not change significantly compared to the control condition (CONTROL). Importantly, these differences between the cold and control temperature could only be significantly characterized by PRVNIRS, but not by PRVPPG. Furthermore, the better performance in characterizing short-term variability of PRVNIRS compared to PRVPPG was not only observed under potentially stressful respiratory challenges (Figs. 6 and 8), but were even detectable under RS conditions (Fig. 5 and Table 2). The ROC analysis confirmed these results indicating that PRVNIRS had a better predictive power to differentiate the temperature change compared to PRVPPG, with the SD1/SD2 ratio obtained from the Poincaré plot revealing the best discrimination (AUC-/ROC-differences, Fig. 7).

Together, our results indicated that PRVNIRS had a significantly higher sensitivity to the short-term contributions of the PSNS compared to PRVPPG. These findings show that under conditions which may induce changes primarily in short-term variability, both research and clinical settings may benefit from using PRVNIRS to overcome the lower reliability of PRVPPG. That the PRVNIRS signal contains more high-frequency information than PRVPPG can also be easily see in Fig. 3.

5.3.

Methodological Considerations and Limitations

Core and skin temperature are the body’s two temperature components. Core temperature (Tc) represents the internal or deep body temperature, whereas skin temperature represents the mean outside surface body temperature (Tsk). The average temperature of the body at any time is a weighted balance between these two temperature components. When confronted with thermal stress (heat or cold), the body strives to control Tc through physiological adjustments, and Tsk provides the major feedback to the brain to coordinate this control.

While Tsk varies greatly with ambient temperature, Tb is relatively stable. When Tsk decreases, HR in general goes down due to a parasympathetic reflex.47 However, if the cold stress is of sufficient magnitude to decrease Tc, HR may either increase (due to sympathetic activation) or decrease (due to increased central blood volume). Regarding the present study, we hypothesized that the cold temperature change was not strong enough to affect Tc (although, this hypothesis could not be confirmed, since we did not directly assess Tsk or Tc). Therefore, the induced cold temperature change in this study was hypothesized to decrease Tsk only. In line with this assumption, we found that HR amplitudes were significantly reduced in response to the cold temperature change (Fig. 3), most likely reflecting a general HR slowdown due to the assumed increase in PSNS activity.8,47

5.4.

Conclusion

By comparing simultaneously acquired PRVNIRS and PRVPPG, the present study showed that PRVNIRS may outperform PRVPPG under conditions involving respiratory and temperature changes. In particular, our results indicated that PRVNIRS may provide a better characterization of the short-term contributions of the autonomous nervous system compared to PRVPPG. Extracting PRVNIRS may, therefore, be advantageous for both research and clinical settings, while being a brain imaging method at the same time.

Acknowledgments

This work has been supported by the career development program Filling the Gap, University of Zurich, Switzerland.

References

1. 

H. V. Huikuri and P. K. Stein, “Heart rate variability in risk stratification of cardiac patients,” Ambul. ECG Monit. Clin. Pract. Res. Appl., 56 153 –159 (2013). Google Scholar

2. 

G. Prinsloo, H. Rauch and W. Derman, “A brief review and clinical application of heart rate variability biofeedback in sports, exercise, and rehabilitation medicine,” Phys. Sportmed., 42 88 –99 (2014). http://dx.doi.org/10.3810/psm.2014.05.2061 Google Scholar

3. 

J. Sacha, “Interaction between heart rate and heart rate variability,” Ann. Noninvasive Electrocardiol., 19 207 –216 (2014). http://dx.doi.org/10.1111/anec.12148 Google Scholar

4. 

C. da Silva et al., “The effect of physical training on heart rate variability in healthy children: a systematic review with meta-analysis,” Pediatr. Exercise Sci., 26 147 –158 (2014). http://dx.doi.org/10.1123/pes.2013-0063 Google Scholar

5. 

Y. Iyriboz et al., “Accuracy of pulse oximeters in estimating heart rate at rest and during exercise,” Br. J. Sports Med., 25 162 –164 (1991). http://dx.doi.org/10.1136/bjsm.25.3.162 BJSMDZ 0306-3674 Google Scholar

6. 

G. Lu and F. Yang, “Limitations of oximetry to measure heart rate variability measures,” Cardiovasc. Eng., 9 119 –125 (2009). http://dx.doi.org/10.1007/s10558-009-9082-3 Google Scholar

7. 

A. Schäfer and J. Vagedes, “How accurate is pulse rate variability as an estimate of heart rate variability? a review on studies comparing photoplethysmographic technology with an electrocardiogram,” Int. J. Cardiol., 166 15 –29 (2013). http://dx.doi.org/10.1016/j.ijcard.2012.03.119 IJCDD5 0167-5273 Google Scholar

8. 

T. Mäkinen et al., “Autonomic nervous function during whole-body cold exposure before and after cold acclimation,” Aviat. Space Environ. Med., 79 875 –882 (2008). http://dx.doi.org/10.3357/ASEM.2235.2008 Google Scholar

9. 

W.-H. Lin et al., “Comparsion of heart rate variability from PPG with that from ECG,” The International Conference on Health Informatics, 42 213 –215 Springer International Publishing, New York (2014). Google Scholar

10. 

P. Grossman and S. Svebak, “Respiratory sinus arrhythmia as an index of parasympathetic cardiac control during active coping,” Psychophysiology, 24 228 –235 (1987). http://dx.doi.org/10.1111/psyp.1987.24.issue-2 PSPHAF 0048-5772 Google Scholar

11. 

P. Grossman, J. Karemaker and W. Wieling, “Prediction of tonic parasympathetic cardiac control using respiratory sinus arrhythmia: the need for respiratory control,” Psychophysiology, 28 201 –216 (1991). http://dx.doi.org/10.1111/psyp.1991.28.issue-2 PSPHAF 0048-5772 Google Scholar

12. 

P. G. Katona and F. Jih, “Respiratory sinus arrhythmia: noninvasive measure of parasympathetic cardiac control,” J. Appl. Physiol., 39 801 –805 (1975). Google Scholar

13. 

A. E. Hedmann et al., “The high frequency component of heart rate variability reflects cardiac parasympathetic modulation rather than parasympathetic ‘tone’,” Acta Physiol. Scand., 155 267 –273 (1995). http://dx.doi.org/10.1111/apha.1995.155.issue-3 Google Scholar

14. 

G. E. Billman, “The LF/HF ratio does not accurately measure cardiac sympatho-vagal balance,” Front. Physiol., 4 26 (2013). FROPBK 0301-536X Google Scholar

15. 

A. Malliani et al., “Cardiovascular neural regulation explored in the frequency domain,” Circulation, 84 482 –492 (1991). http://dx.doi.org/10.1161/01.CIR.84.2.482 CIRCAZ 0009-7322 Google Scholar

16. 

M. Pagani et al., “Power spectral density of heart rate variability as an index of sympatho-vagal interaction in normal and hypertensive subjects,” J. Hypertens., 2 S383 –S385 (1984). JOHYD3 0263-6352 Google Scholar

17. 

M. Pagani et al., “Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog,” Circ. Res., 59 178 –193 (1986). http://dx.doi.org/10.1161/01.RES.59.2.178 CIRUAL 0009-7330 Google Scholar

18. 

M. Doret et al., “Fractal analysis and hurst parameter for intrapartum fetal heart rate variability analysis: a versatile alternative to frequency bands and LF/HF ratio,” PLoS ONE, 10 e0136661 (2015). http://dx.doi.org/10.1371/journal.pone.0136661 POLNCL 1932-6203 Google Scholar

19. 

D. Saboul, V. Pialoux and C. Hautier, “The breathing effect of the LF/HF ratio in the heart rate variability measurements of athletes,” Eur. J. Sport Sci., 14 S282 –S288 (2014). http://dx.doi.org/10.1080/17461391.2012.691116 Google Scholar

20. 

H. Wang and S. Huang, “SDNN/RMSSD as a surrogate for LF/HF: a revised investigation,” Model. Simul. Eng., 2012 931943 (2012). http://dx.doi.org/10.1155/2012/931943 MSMEEU 0965-0393 Google Scholar

21. 

R. Balocchi et al., “Revisiting the potential of time-domain indexes in short-term HRV analysis,” Biomed. Tech., 51 190 –193 (2006). http://dx.doi.org/10.1515/BMT.2006.034 Google Scholar

22. 

M. Brennan, M. Palaniswami and P. Kamen, “Do existing measures of Poincare plot geometry reflect nonlinear features of heart rate variability?,” IEEE Trans. Biomed. Eng., 48 1342 –1347 (2001). http://dx.doi.org/10.1109/10.959330 IEBEAX 0018-9294 Google Scholar

23. 

C. K. Karmakar et al., “Complex correlation measure: a novel descriptor for Poincaré plot,” Biomed. Eng. OnLine, 8 17 (2009). http://dx.doi.org/10.1186/1475-925X-8-17 Google Scholar

24. 

C. K. Karmakar et al., “Sensitivity of temporal heart rate variability in Poincaré plot to changes in parasympathetic nervous system activity,” Biomed. Eng. OnLine, 10 17 (2011). http://dx.doi.org/10.1186/1475-925X-10-17 Google Scholar

25. 

I. Trajkovic, F. Scholkmann and M. Wolf, “Estimating and validating the interbeat intervals of the heart using near-infrared spectroscopy on the human forehead,” J. Biomed. Opt., 16 087002 (2011). http://dx.doi.org/10.1117/1.3606560 JBOPFO 1083-3668 Google Scholar

26. 

K. L. Perdue et al., “Extraction of heart rate from functional near-infrared spectroscopy in infants,” J. Biomed. Opt., 19 067010 (2014). http://dx.doi.org/10.1117/1.JBO.19.6.067010 JBOPFO 1083-3668 Google Scholar

27. 

H. ChuDuc, K. NguyenPhan and D. NguyenViet, “A review of heart rate variability and its applications,” in 3rd Int. Conf. Biomedical Engineering Technology (ICBET 2013), 80 –85 (2013). Google Scholar

28. 

A. Singh et al., “Spatial registration of multichannel multi-subject fNIRS data to MNI space without MRI,” NeuroImage, 27 842 –851 (2005). http://dx.doi.org/10.1016/j.neuroimage.2005.05.019 NEIMEF 1053-8119 Google Scholar

29. 

M. Xia, J. Wang and Y. He, “BrainNet viewer: a network visualization tool for human brain connectomics,” PLoS ONE, 8 e68910 (2013). http://dx.doi.org/10.1371/journal.pone.0068910 POLNCL 1932-6203 Google Scholar

30. 

F. Scholkmann, J. Boss and M. Wolf, “An efficient algorithm for automatic peak detection in noisy periodic and quasi-periodic signals,” Algorithms, 5 588 –603 (2012). http://dx.doi.org/10.3390/a5040588 1748-7188 Google Scholar

31. 

Task force of the European Society of Cardiology the North American Society of Pacing Electrophysiology, “Heart rate variability: standards of measurement, physiological interpretation, and clinical use,” Circulation, 93 1043 –1065 (1996). http://dx.doi.org/10.1161/01.CIR.93.5.1043 CIRCAZ 0009-7322 Google Scholar

32. 

D. Singh et al., “Effects of RR segment duration on HRV spectrum estimation,” Physiol. Meas., 25 721 –735 (2004). http://dx.doi.org/10.1088/0967-3334/25/3/012 PMEAE3 0967-3334 Google Scholar

33. 

C. C. Grant et al., “Importance of tachogram length and period of recording during noninvasive investigation of the autonomic nervous system,” Ann. Noninvasive Electrocardiol., 16 131 –139 (2011). http://dx.doi.org/10.1111/anec.2011.16.issue-2 Google Scholar

34. 

S. M. Pincus, “Approximate entropy as a measure of system complexity,” Proc. Natl. Acad. Sci., 88 2297 –2301 (1991). http://dx.doi.org/10.1073/pnas.88.6.2297 Google Scholar

35. 

P. Li et al., “Testing pattern synchronization in coupled systems through different entropy-based measures,” Med. Biol. Eng. Comput., 51 581 –591 (2013). http://dx.doi.org/10.1007/s11517-012-1028-z MBECDY 0140-0118 Google Scholar

36. 

T. Zhang, Z. Yang and J. Coote, “Cross-sample entropy statistic as a measure of complexity and regularity of renal sympathetic nerve activity in the rat,” Exp. Physiol., 92 659 –669 (2007). http://dx.doi.org/10.1113/expphysiol.2007.037150 EXPHEZ 0958-0670 Google Scholar

37. 

M. Aktaruzzaman and R. Sassi, “Parametric estimation of sample entropy in heart rate variability analysis,” Biomed. Signal Process. Control, 14 141 –147 (2014). http://dx.doi.org/10.1016/j.bspc.2014.07.011 Google Scholar

38. 

D. E. Lake et al., “Sample entropy analysis of neonatal heart rate variability,” Am. J. Physiol. Regul. Integr. Comp. Physiol., 283 R789 –R797 (2002). http://dx.doi.org/10.1152/ajpregu.00069.2002 Google Scholar

39. 

M. Weippert et al., “Sample entropy and traditional measures of heart rate dynamics reveal different modes of cardiovascular control during low intensity exercise,” Entropy, 16 5698 –5711 (2014). http://dx.doi.org/10.3390/e16115698 ENTRFG 1099-4300 Google Scholar

40. 

Y. İşler and M. Kuntalp, “Combining classical HRV indices with wavelet entropy measures improves to performance in diagnosing congestive heart failure,” Comput. Biol. Med., 37 1502 –1510 (2007). Google Scholar

41. 

J. Ramshur, Design, Evaluation, and Application of Heart Rate Variability Analysis Software (HRVAS), University of Memphis, Memphis, Tennessee (2010). Google Scholar

42. 

M. R. Esco and A. A. Flatt, “Ultra-short-term heart rate variability indexes at rest and post-exercise in athletes: evaluating the agreement with accepted recommendations,” J. Sports Sci. Med., 13 535 –541 (2014). Google Scholar

43. 

T. Thong et al., “Accuracy of ultra-short heart rate variability measures,” in Engineering in Medicine and Biology Society, 2003. Proc. of the 25th Annual Int. Conf. of the IEEE, 2424 –2427 (2003). http://dx.doi.org/10.1109/IEMBS.2003.1280405 Google Scholar

44. 

C. K. Karmakar et al., “Analyzing temporal variability of standard descriptors of Poincaré plots,” J. Electrocardiol., 43 719 –724 (2010). http://dx.doi.org/10.1016/j.jelectrocard.2010.09.001 JECAB4 0022-0736 Google Scholar

45. 

M. Bolanos, H. Nazeran and E. Haltiwanger, “Comparison of heart rate variability signal features derived from electrocardiography and photoplethysmography in healthy individuals,” in Engineering in Medicine and Biology Society, 2006. EMBS ‘06. 28th Annual Int. Conf. of the IEEE, 4289 –4294 (2006). http://dx.doi.org/10.1109/IEMBS.2006.260607 Google Scholar

46. 

N. Selvaraj et al., “Assessment of heart rate variability derived from finger-tip photoplethysmography as compared to electrocardiography,” J. Med. Eng. Technol., 32 479 –484 (2008). http://dx.doi.org/10.1080/03091900701781317 JMTEDN 0309-1902 Google Scholar

47. 

J. LeBlanc, Man in the Cold, Charles C Thomas Publishing, Springfield, IL (1975). Google Scholar

Biography

Lisa Holper is a resident physician at the Department of Psychiatry, Psychotherapy, and Psychosomatics, Hospital of Psychiatry Zurich, University Zurich. She has published and contributed to over 30 papers addressing human research in healthy and psychiatric populations, particularly in the field of optical brain imaging.

Erich Seifritz is the director of the Department of Psychiatry, Psychotherapy, and Psychosomatics, Hospital of Psychiatry Zurich, University Zurich. He has published and contributed to over 100 papers addressing animal and human research on psychiatric populations in the fields of neuroimaging, brain stimulation, genetics, and neuroeconomics.

Felix Scholkmann is a postdoctoral researcher at the Biomedical Optics Research Laboratory, University Hospital Zurich, University of Zurich. He has published and contributed to over 30 papers addressing the technical development and application of fNIRS-based optical brain imaging and physiological monitoring.

© 2016 Society of Photo-Optical Instrumentation Engineers (SPIE) 1083-3668/2016/$25.00 © 2016 SPIE
Lisa Holper M.D., Erich Seifritz M.D., and Felix Scholkmann "Short-term pulse rate variability is better characterized by functional near-infrared spectroscopy than by photoplethysmography," Journal of Biomedical Optics 21(9), 091308 (17 May 2016). https://doi.org/10.1117/1.JBO.21.9.091308
Published: 17 May 2016
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Cited by 12 scholarly publications.
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KEYWORDS
Near infrared spectroscopy

Remote sensing

Temperature metrology

Nervous system

Photoplethysmography

Electrocardiography

Statistical analysis

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